The reorganization of corticomuscular coherence during a transition between sensorimotor states

Highlights

• We investigate corticomuscular coherence during transitions in sensorimotor state.

• During transitions coherence changed from the beta band to the alpha and gamma bands.

• Alpha- and gamma-band coherence was only observed during movement overshoot.

• Alpha-band and gamma-band reflect afferent and efferent corticospinal interactions.

• Dual-band synchronization may be involved in parsing prediction errors.

Abstract

Recent research suggests that neural oscillations in different frequency bands support distinct and sometimes parallel processing streams in neural circuits. Studies of the neural dynamics of human motor control have primarily focused on oscillations in the beta band (15–30 Hz). During sustained muscle contractions, corticomuscular coherence is mainly present in the beta band, while coherence in the alpha (8–12 Hz) and gamma (30–80 Hz) bands has not been consistently found. Here we test the hypothesis that the frequency of corticomuscular coherence changes during transitions between sensorimotor states. Corticomuscular coherence was investigated in twelve participants making rapid transitions in force output between two targets. Corticomuscular coherence was present in the beta band during sustained contractions but vanished before movement onset, being replaced by transient synchronization in the alpha and gamma bands during dynamic force output. Analysis of the phase spectra suggested a time delay from muscle to cortex for alpha-band coherence, by contrast to a time delay from cortex to muscle for gamma-band coherence, indicating afferent and efferent corticospinal interactions respectively. Moreover, alpha and gamma-band coherence revealed distinct spatial topologies, suggesting different generative mechanisms. Coherence in the alpha and gamma bands was almost exclusively confined to trials showing a movement overshoot, suggesting a functional role related to error correction. We interpret the dual-band synchronization in the alpha and gamma bands as parallel streams of corticospinal processing involved in parsing prediction errors and generating new motor predictions.

Introduction

Synchronous brain rhythms represent a dynamic mechanism for coordinating neural activity across large-scale neuronal networks and controlling the timing of neuronal firing (Buzsaki and Draguhn, 2004, Engel et al., 2001, Wang, 2010). Evidence from the past two decades of research suggests that neural oscillations subserve important cognitive functions, including motor control (Fetz, 2013, Fries, 2005, Schnitzler and Gross, 2005). During sustained contractions, primary motor cortex shows oscillations in alpha (8–12 Hz) and beta (15–30 Hz) bands (Baker et al., 2003, Murthy and Fetz, 1992, Sanes and Donoghue, 1993). Although oscillations in both frequency bands are effectively carried down the corticospinal tract (Baker et al., 2003), most studies using sustained contractions find that only beta-band oscillations are coherent between motor cortex and muscle activity (Baker et al., 1997, Conway et al., 1995, Gross et al., 2000, Halliday et al., 1998). Corticomuscular beta-band coherence is most prominent during tonic muscle contractions and disappears during movement (Baker et al., 1997, Baker et al., 1999, Kilner et al., 2000, Riddle and Baker, 2006) and beta-band activity is enhanced when higher precision is required (Gilbertson et al., 2005, Kristeva et al., 2007, Kristeva-Feige et al., 2002, Witte et al., 2007). These findings suggest that the beta-band activity is related to a mechanism that maintains the current sensorimotor state (Baker, 2007, Engel and Fries, 2010, Van Wijk et al., 2012).

Research findings of corticomuscular coherence at other frequencies are inconclusive. A few studies have reported alpha-band coherence during sustained contractions (Raethjen et al., 2002) and during slow finger movements (Gross et al., 2002, Williams et al., 2009). It has recently been proposed that a spinal circuit may reduce 10-Hz oscillations in descending cortical input to the spinal motor neurons (Williams et al., 2010). In particular, computational analyses have shown that recurrent inhibition via Renshaw cells in the spinal cord leads to partial cancellation of 10 Hz oscillations, markedly reducing corticomuscular coherence at this frequency (Williams and Baker, 2009). Corticomuscular gamma-band coherence has been observed during dynamic force output (Cheyne et al., 2008, Omlor et al., 2007), as well as during movement preparation (Schoffelen et al., 2005, Schoffelen et al., 2011). These results indicate that the frequency of corticomuscular coherence varies across motor tasks and may hence be dependent on the moment-to-moment motor state (Marsden et al., 2000).

An overarching framework suggests that different carrier frequencies reflect different types of neural processing, predicting changes in the frequency of corticomuscular coherence during transitions in sensorimotor state, e.g. from sustained contractions to dynamic force output (Engel and Fries, 2010). Here we test this hypothesis by investigating corticomuscular coherence while participants make fast transitions between two distinct force levels. We hypothesized that corticomuscular coherence in the beta band would disappear during dynamic motor output and that coherence at other frequencies would appear during the transition between force levels. Phase spectra are used to characterize the type of interaction underlying the observed functional connectivity. Capturing the reorganization of the dynamics in the sensorimotor loop speaks to the functional role of corticomuscular coherence and its role in coordinating the information transfer between sensorimotor cortex and spinal populations.